Redox-dependent induction of antioxidant defenses by phenolic diterpenes confers stress tolerance in normal human skin fibroblasts: Insights on replicative senescence

Free Radical Biology and Medicine

Volumn 83, Issue , 2015, Pages 262-272

  Carvalho, Ana C ^a,b   Gomes, Andreia C ^b   Pereira Wilson, Cristina ^a   Lima, Cristovao F ^a  

^a UNIVERSITY OF TRÁS OS MONTES AND ALTO DOURO   (Portugal)

^b UNIVERSITY OF MINHO   (Portugal)

Author keywords

Aging; Cytoprotection; Normal humanskin fibroblasts; Nrf2; Phenolic diterpenes

Indexed keywords

ANTIOXIDANT; CARNOSIC ACID; CARNOSOL; CYTOPROTECTIVE AGENT; HYDROGEN PEROXIDE; TERT BUTYL HYDROPEROXIDE; TRANSCRIPTION FACTOR NRF2; ABIETANE DERIVATIVE; MESSENGER RNA; PLANT EXTRACT;

ADULT; ANTIOXIDANT ACTIVITY; ARTICLE; BREAST BIOPSY; CELL AGING; CELL DIVISION; CELL STRESS; CONTROLLED STUDY; DIPLOIDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; NORMAL HUMAN; OXIDATION REDUCTION STATE; PRIORITY JOURNAL; SENESCENCE; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; APOPTOSIS; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; ENZYME IMMUNOASSAY; FIBROBLAST; GENETICS; METABOLISM; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN; WESTERN BLOTTING;

ADULT; ANTIOXIDANTS; APOPTOSIS; BLOTTING, WESTERN; CELL AGING; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DITERPENES, ABIETANE; FEMALE; FIBROBLASTS; HUMANS; IMMUNOENZYME TECHNIQUES; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; OXIDATIVE STRESS; PLANT EXTRACTS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SKIN;

EID: 84928377727     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.02.022     Document Type: Article

References (66)

1. United Nations World population ageing: 1950-2050 2001 United Nations New York
2. H. Stefánsson The science of ageing and anti-ageing EMBO Rep. 6 2005 S1 S3
3. P.U. Giacomoni Ageing, science and the cosmetics industry EMBO Rep. 6 2005 S45 S48
4. S.I. Aging Rattan intervention, prevention, and therapy through hormesis J. Gerontol. A Biol. Sci. Med. Sci 59 2004 705 709
5. S.I. Rattan Anti-ageing strategies: prevention or therapy? EMBO Rep 6 2005 S25 S29
6. S.I. Hormesis Rattan in aging Ageing Res. Rev. 7 2008 63 78
7. E.J. Calabrese, K.A. Bachmann, A.J. Bailer, P.M. Bolger, J. Borak Biological stress response terminology: integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework Toxicol. Appl. Pharmacol. 222 2007 122 128
8. M.P. Mattson Hormesis defined Ageing Res. Rev. 7 2008 1 7
9. Z. Radak, H.Y. Chung, E. Koltai, A.W. Taylor, and S. Goto Exercise, oxidative stress and hormesis Ageing Res. Rev. 7 2008 34 42
10. M.P. Mattson Dietary factors, hormesis and health Ageing Res. Rev. 7 2008 43 48
11. B.J. Morris How xenohormetic compounds confer health benefits E. Le Bourg, S.I. Rattan, Mild stress and healthy aging: applying hormesis in aging research and interventions 2008 Springer Science + Business Media B.V. Dordrecht 115 138
12. C.F. Lima, C. Pereira-Wilson, and S.I. Rattan Curcumin induces heme oxygenase-1 in normal human skin fibroblasts through redox signaling: relevance for anti-aging intervention Mol. Nutr. Food Res. 55 2011 430 442
13. V. Calabrese, C. Cornelius, A.T. Dinkova-Kostova, I. Iavicoli, R. Di Paola, A. Koverech, S. Cuzzocrea, E. Rizzarelli, and E.J. Calabrese Cellular stress responses, hormetic phytochemicals and vitagenes in aging and longevity Biochim. Biophys. Acta 1822 2012 753 783
14. S.I. Rattan Rationale and methods of discovering hormetins as drugs for healthy ageing Expert Opin. Drug Discov 7 2012 439 448
15. S.I. Rattan, V. Kryzch, S. Schnebert, E. Perrier, and C. Nizard Hormesis-based anti-aging products: a case study of a novel cosmetic Dose Response 11 2013 99 108
16. S.I. Rattan Molecular gerontology: from homeodynamics to hormesis Curr. Pharm. Des 20 2014 3036 3039
17. T.G. Son, S. Camandola, and M.P. Mattson Hormetic dietary phytochemicals Neuromol. Med. 10 2008 236 246
18. Y.J. Surh, J.K. Kundu, and H.K. Na Nrf2 as a master redox switch in turning on the cellular signaling involved in the induction of cytoprotective genes by some chemopreventive phytochemicals Planta Med. 74 2008 1526 1539
19. H. Motohashi, and M. Yamamoto Nrf2-Keap1 defines a physiologically important stress response mechanism Trends Mol. Med. 10 2004 549 557
20. M. Kobayashi, and M. Yamamoto Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species Adv. Enzyme Regul. 46 2006 113 140
21. J.H. Suh, S.V. Shenvi, B.M. Dixon, H. Liu, A.K. Jaiswal, R.M. Liu, and T.M. Hagen Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid Proc. Natl. Acad. Sci. USA 101 2004 3381 3386
22. M. Suzuki, T. Betsuyaku, Y. Ito, K. Nagai, Y. Nasuhara, K. Kaga, S. Kondo, and M. Nishimura Down-regulated NF-E2-related factor 2 in pulmonary macrophages of aged smokers and patients with chronic obstructive pulmonary disease Am. J. Respir. Cell Mol. Biol. 39 2008 673 682
23. A.J. Przybysz, K.P. Choe, L.J. Roberts, and K. Strange Increased age reduces DAF-16 and SKN-1 signaling and the hormetic response of Caenorhabditis elegans to the xenobiotic juglone Mech. Ageing Dev. 130 2009 357 369
24. M.M. Rahman, G.P. Sykiotis, M. Nishimura, R. Bodmer, and D. Bohmann Declining signal dependence of Nrf2-MafS-regulated gene expression correlates with aging phenotypes Aging Cell 12 2013 554 562
25. G.P. Sykiotis, and D. Bohmann Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila Dev. Cell 14 2008 76 85
26. K.N. Lewis, J. Mele, J.D. Hayes, and R. Buffenstein Nrf2, a guardian of healthspan and gatekeeper of species longevity Integr. Comp. Biol. 50 2010 829 843
27. H.M. Crook-McMahon, M. Oláhová, E.L. Button, J.J. Winter, and E.A. Veal Genome-wide screening identifies new genes required for stress-induced phase 2 detoxification gene expression in animals BMC Biol 12 2014 64
28. D. Martin, A.I. Rojo, M. Salinas, R. Diaz, G. Gallardo, J. Alam, C.M. De Galarreta, and A. Cuadrado Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol J. Biol. Chem. 279 2004 8919 8929
29. T. Satoh, K. Kosaka, K. Itoh, A. Kobayashi, M. Yamamoto, Y. Shimojo, C. Kitajima, J. Cui, J. Kamins, S. Okamoto, M. Izumi, T. Shirasawa, and S.A. Lipton Carnosic acid, a catecholtype electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of specific cysteines J. Neurochem. 104 2008 1131 1161
30. T. Satoh, M. Izumi, Y. Inukai, Y. Tsutsumi, N. Nakayama, K. Kosaka, Y. Shimojo, C. Kitajima, K. Itoh, T. Yokoi, and T. Shirasawa Carnosic acid protects neuronal HT22 cells through activation of the antioxidant-responsive element in free carboxylic acid- and catechol hydroxyl moieties-dependent manners Neurosci. Lett. 434 2008 260 265
31. D.C. Kraft, C.C. Deocaris, and S.I. Rattan Proteasomal oscillation during mild heat shock in aging human skin fibroblasts Ann. N. Y. Acad. Sci 1067 2006 224 227
32. V.J. Cristofalo, R.G. Allen, R.J. Pignolo, B.G. Martin, and J.C. Beck Relationship between donor age and the replicative lifespan of human cells in culture: a reevaluation Proc. Natl. Acad. Sci. USA 95 1998 10614 10619
33. M.E. Anderson Determination of glutathione and glutathione disulfide in biological samples Methods Enzymol. 113 1985 548 555
34. C.F. Lima, M. Fernandes-Ferreira, and C. Pereira-Wilson Phenolic compounds protect HepG2 cells from oxidative damage: relevance of glutathione levels Life Sci. 79 2006 2056 2068
35. M.W. Pfaffl A new mathematical model for relative quantification in real-time RT-PCR Nucleic Acids Res. 29 2001 e45
36. C.F. Lima, P.B. Andrade, R.M. Seabra, M. Fernandes-Ferreira, and C. Pereira-Wilson The drinking of a Salvia officinalis infusion improves liver antioxidant status in mice and rats J. Ethnopharmacol. 97 2005 383 389
37. C.P. Xavier, C.F. Lima, A. Preto, R. Seruca, M. Fernandes-Ferreira, and C. Luteolin Pereira-Wilson quercetin and ursolic acid are potent inhibitors of proliferation and inducers of apoptosis in both KRAS and BRAF mutated human colorectal cancer cells Cancer Lett. 281 2009 162 170
38. E.R. Nielsen, Y.E. Eskildsen-Helmond, and S.I. Rattan MAP kinases and heat shock-induced hormesis in human fibroblasts during serial passaging in vitro Ann. N. Y. Acad. Sci 1067 2006 343 348
39. J.H. Chen, S.E. Ozanne, and C.N. Hales Methods of cellular senescence induction using oxidative stress T.O. Tollefsbol, Biological aging: methods and protocols. methods in molecular biology volume 371 2007 Humana Press NJ 179 189
40. C. Martin-Ruiz, G. Saretzki, J. Petrie, J. Ladhoff, J. Jeyapalan, W. Wei, J. Sedivy, and T. von Zglinicki Stochastic variation in telomere shortening rate causes heterogeneity of human fibroblast replicative life span J. Biol. Chem. 279 2004 17826 17833
41. K.C. Lian, J.J. Chuang, C.W. Hsieh, B.S. Wung, G.D. Huang, T.Y. Jian, and Y.W. Sun Dual mechanisms of NF-κB inhibition in carnosol-treated endothelial cells Toxicol. Appl. Pharmacol. 245 2010 21 35
42. T. Takahashi, T. Tabuchi, Y. Tamaki, K. Kosaka, Y. Takikawa, and T. Satoh Carnosic acid and carnosol inhibit adipocyte differentiation in mouse 3T3-L1 cells through induction of phase2 enzymes and activation of glutathione metabolism Biochem. Biophys. Res. Commun. 382 2009 549 554
43. Q.M. Chen, V.C. Tu, J. Catania, M. Burton, O. Toussaint, and T. Dilley Involvement of Rb family proteins, focal adhesion proteins and protein synthesis in senescent morphogenesis induced by hydrogen peroxide J. Cell Sci. 113 2000 4087 4097
44. S.I.S. Rattan, R.A. Fernandes, D. Demirovic, B. Dymek, and C.F. Lima Heat stress and hormetin-induced hormesis in human cells: effects on aging, wound healing, angiogenesis and differentiation Dose-Response 7 2009 90 103
45. P. Verbeke, B.F. Clark, and S.I. Rattan Reduced levels of oxidized and glycoxidized proteins in human fibroblasts exposed to repeated mild heat shock during serial passaging in vitro Free Radic. Biol. Med. 31 2001 1593 1602
46. J. Fonager, R. Beedholm, B.F. Clark, and S.I. Rattan Mild stress-induced stimulation of heat-shock protein synthesis and improved functional ability of human fibroblasts undergoing aging in vitro Exp. Gerontol. 37 2002 1223 1228
47. C.C. Chen, H.L. Chen, C.W. Hsieh, Y.L. Yang, and B.S. Wung Upregulation of NF-E2-related factor-2-dependent glutathione by carnosol provokes a cytoprotective response and enhances cell survival Acta Pharmacol. Sin. 32 2011 62 69
48. H. Zhang, and H.J. Forman Glutathione synthesis and its role in redox signaling Semin. Cell Dev. Biol. 23 2012 722 728
49. I. Rebrin, and R.S. Sohal Pro-oxidant shift in glutathione redox state during aging Adv. Drug Deliv. Rev. 60 2008 1545 1552
50. J. Lu, and A. Holmgren The thioredoxin antioxidant system Free Radic. Biol. Med. 66 2014 75 87
51. S.L. Richheimer, M.W. Bernart, G.A. King, M.C. Kent, and D.T. Beiley Antioxidant activity of lipid-soluble phenolic diterpenes from rosemary J. Am. Oil Chem. 73 1996 507 514 Soc 73 1996 507 514
52. T. Satoh, S.R. McKercher, and S.A. Lipton Nrf2/ARE-mediated antioxidant actions of pro-electrophilic drugs Free Radic. Biol. Med. 65 2013 645 657
53. N. Ballatori, S.M. Krance, S. Notenboom, S. Shi, K. Tieu, and C.L. Hammond Glutathione dysregulation and the etiology and progression of human diseases Biol. Chem. 390 2009 191 214
54. D. Demirovic, and S.I. Rattan Establishing cellular stress response profiles as biomarkers of homeodynamics, health and hormesis Exp. Gerontol. 48 2013 94 98
55. D. Demirovic, I.M. deToda, C. Nizard, and S.I. Rattan Differential translocation of heat shock factor-1 after mild and severe stress to human skin fibroblasts undergoing aging in vitro. J. Cell Commun. Signal. 8 2014 333 339
56. G.P. Dimri What has senescence got to do with cancer? Cancer Cell 7 2005 505 512
57. E.S. Hwang, G. Yoon, and H.T. Kang A comparative analysis of the cell biology of senescence and aging Cell. Mol. Life Sci. 66 2009 2503 2524
58. G.P. Dimri, X. Lee, G. Basile, M. Acosta, G. Scott, C. Roskelley, E.E. Medrano, M. Linskens, I. Rubelj, and O. Pereira-Smith A biomarker that identifies senescent human cells in culture and in aging skin in vivo Proc. Natl. Acad. Sci. USA 92 1995 9363 9367
59. M. Narita, S. N͡nez, E. Heard, M. Narita, A.W. Lin, S.A. Hearn, D.L. Spector, G.J. Hannon, and S.W. Lowe Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence Cell 113 2003 703 716
60. J.G. Wood, B. Rogina, S. Lavu, K. Howitz, S.L. Helfand, M. Tatar, and D. Sinclair Sirtuin activators mimic caloric restriction and delay ageing in metazoans Nature 430 2004 686 689
61. D.R. Valenzano, E. Terzibasi, T. Genade, A. Cattaneo, L. Domenici, and A. Cellerino Resveratrol prolongs lifespan and retards the onset of age-related markers in a short-lived vertebrate Curr. Biol. 16 2006 296 300
62. M.A. Wilson, B. Shukitt-Hale, W. Kalt, D.K. Ingram, J.A. Joseph, and C.A. Wolkow Blueberry polyphenols increase lifespan and thermotolerance in Caenorhabditis elegans Aging Cell 5 2006 59 68
63. L.K. Heilbronn, and E. Ravussin Calorie restriction and aging: review of the literature and implications for studies in humans Am. J. Clin. Nutr. 78 2003 361 369
64. Y. Niu, L. Na, R. Feng, L. Gong, Y. Zhao, Q. Li, Y. Li, and C. Sun The phytochemical, EGCG, extends lifespan by reducing liver and kidney function damage and improving age-associated inflammation and oxidative stress in healthy rats Aging Cell 12 2013 1041 1049
65. S. Qin, J. Chen, S. Tanigawa, and D.X. Hou Gene expression profiling and pathway network analysis of hepatic metabolic enzymes targeted by baicalein J. Ethnopharmacol. 140 2012 131 140
66. F. Zhang, W. Wang, Y. Tsuji, S.V. Torti, and F.M. Torti Post-transcriptional modulation of iron homeostasis during p53-dependent growth arrest J. Biol. Chem. 283 2008 33911 33918